Cropsaver
Journal of Plant Protection
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78 Cite this as: Nasahi C, Amatullah HL, & Kurniadie D. 2023. Effect of fobio on intensity of moler disease (Fusarium
oxysporum) on various shallot cultivars. Cropsaver: Journal of Plant Protection, 6(2): 78-85.
https://doi.org/10.24198/cropsaver.v6i2.47087
Antagonistic Endophytic Fungi from Papaya Fruit Against Anthracnose Causing Pathogens (Colletotrichum gloeosporioides) on Papaya Fruit
Ceppy Nasahi1*, Hana Lathifah Amatullah1, & Denny Kurniadie2
Department of Plant Pests and Diseases, Faculty of Agriculture, Universitas Padjadjaran, Jatinangor, West Java, Indonesia, 45363
Department of Agronomy, Faculty of Agriculture, Universitas Padjadjaran, Jatinangor, West Java, Indonesia, 45363
*Corresponding Author: [email protected]
Received May 26, 2023; revised July 09, 2023; accepted October 27, 2023
ABSTRACT
Anthracnose disease caused by Colletotrichum gloeosporioides considered a major disease on papaya fruit. One way to control plant diseases is to use antagonistic fungi as biocontrol agents. Several antagonistic fungi can be found in plant tissues (endophytic fungi). This study aims to get endophytic fungi from papaya fruit antagonistic to the fungus C. gloeosporioides.
The research used a Completely Randomized Design (CRD) consisting of four treatments and five replications on in-vitro and in-vivo tests. The results showed that three isolates of endophytic fungi found from papaya fruit were Fusarium sp., Aureobasidium sp., and Acremonium sp., which had an inhibition of 63.5%, 67.86%, and 7.52%, respectively. Fusarium sp.
and Aureobasidium sp. are potentially considered antagonist fungi in controlling the fungus C. gloeosporioides in in-vitro testing based on the inhibition results were more than 60%. Aureobasidium sp. is considered potential antagonist fungi according to the colonization or growth of C. gloeosporioides mycelium inhibition that emerges on papaya up to 97%.
Keywords: Acremonium sp, biocontrol agent, Aureobasidium sp., Fusarium sp.
Jamur Endofit Antagonis pada Buah Pepaya terhadap Patogen Penyebab Antraknosa (Colletotrichum gloeosporioides) pada Buah Pepaya
ABSTRAK
Penyakit antraknosa yang disebabkan oleh jamur Colletotrichum gloeosporioides merupakan penyakit utama pada buah pepaya. Salah satu cara pengendalian penyakit tanaman adalah dengan menggunakan jamur antagonis sebagai agen biokontrol.
Beberapa jamur antagonis dapat ditemukan di dalam jaringan tanaman (jamur endofit). Penelitian ini bertujuan untuk mendapatkan jamur endofit dari buah pepaya yang bersifat antagonistik terhadap jamur C. gloeosporioides. Penelitian ini menggunakan Rancangan Acak Lengkap, yang terdiri atas empat perlakuan dan lima ulangan pada pengujian secara in-vitro dan in-vivo. Hasil dari penelitian menunjukkan adanya tiga isolat jamur endofit dari buah pepaya, yaitu Fusarium sp.
Aureobasidium sp., dan Acremonium sp. dengan daya hambat berturut-turut 63,5%, 67,86%, dan 7,52%. Fusarium sp. dan Aureobasidium sp. merupakan jamur antagonis yang potensial dalam mengendalikan jamur C. gloeosporioides pada pengujian secara in-vitro berdasarkan hasil daya hambat yang lebih besar dari 60%. Aureobasidium sp. merupakan isolat jamur antagonis potensial berdasarkan kemampuannya dalam menghambat kolonisasi atau pertumbuhan miselium C. gloeosporioides pada buah pepaya dengan penghambatan mencapai 97%.
Kata Kunci: Acremonium sp, agen biokontrol, Aureobasidium sp., Fusarium sp.
INTRODUCTION
Indonesia is one of the main producers of the tropical fruit papaya (Vieira et al., 2022). Indonesia harvests papaya up to 2 tons per hectare monthly (Demak Regency Agriculture and Food Service, 2021).
On the other hand, papaya fruit production in Indonesia decreased by 3.23% in 2017 (Indonesia Central Bureau of Statistics, 2021). The number of papaya fruit decreased because it has a short shelf life and is attacked by anthracnose disease (Wiyono and
Manuwoto, 2008). Pathogenic fungi from the genus Colletotrichum cause anthracnose disease. In general, the Colletotrichum fungus has six main species Colletotrichum gloeosporioides, C. capsici, C.
dematium, C. coccodes, C. acutatum, and Glomerella cingulate (Kim et al., 1999).
Colletotrichum gloeosprorioides is a pre and post-harvest disease which causes 40-100% economic losses in developing countries (Ademe et al., 2013).
The symptoms can be seen from sunken areas and
79 water-soaked spots, rapidly expanding, and the infected tissue becomes soft and necrotic (Ayón-Reyna et al., 2017). Therefore, controlling C.
gloeosprorioides on papaya fruit is necessary, considering the vital effects and losses. Despite using fungicides that affect health and the environment, biological control can be a good option.
Disease management control using biological agents is the most carried out on post-harvest products.
Endophytic fungi are microorganisms that live in plant tissues such as leaves, fruits, twigs, and plant roots, in more than one isolate, different endophytic fungi can be produced from one host plant (Istifadah & Suganda, 2010). Siddiqui & Shaukat (2003) stated that endophytic microorganisms have many benefits as biological agents because some are easily cultured in vitro, can increase plant resistance to parasites, do not attack or produce toxins in plants, and produce growth- stimulating hormones.
Some endophytic fungi can be used as biological agents against the cause of anthracnose disease in some fruits and vegetables. According to Siregar et al. (2007), Bacillus polymyxa bacteria and Trichoderma harzianum as and endofit fungi controlled the pathogen that causes anthracnose in chilli plants. The statement is reinforced by the statement of Zivkovic et al. (2010) that T. harzianum and Gliocladium roseum are endophytic microbes that can be used as biological agents against C. acutatum and C. gloeosporioides that cause anthracnose in fruits.
Study evidence on endophytic fungi Trichoderma sp. successfully suppresses C.
gloesoprorioides fungi in chilli peppers was shown by Herwidyanti et al. (2013). Another study using Aspergillus fungus on chilli fruit also slowed the incubation period of anthracnose disease caused by C.
gloeosporioides (Amaike & Keller, 2011). There has
been no study on endophytic fungi from within papaya fruit tissue, which triggered the author to research the antagonistic potential of endophytic fungi against pathogens that cause anthracnose (C. gloesoprorioides) in post-harvest papaya fruit in vitro and in-vivo.
MATERIALS AND METHODS
The study was conducted at the Laboratory of Biotechnology Plant Protection, Department of Pests and Plant Diseases, Faculty of Agriculture, Universitas Padjadjaran, Sumedang Regency, West Java, Indonesia. Research was conducted from April to June 2022.
Colletotrichum gloeosporioides preparation
Papaya peel was cut 2x2 cm between symptomatic and healthy parts. Furthermore, the cut results are sterilized by soaking in 2% Clorox for a minute and rinsed using sterile aquades. It was then soaked again using 70% alcohol for 30 seconds. After that, the fruit pieces are drained using sterile filter paper. After dryed, the papaya skin is cut back into 1x1 cm in size.
The papaya fruit pieces are placed in prepared Potato Dextrose Agar (PDA) media, added with 0.5%
Chloramphenicol antibiotic, and incubated at room temperature for several days. The pure cultures of C.
gloeosporioides isolates were identified macroscopically and microscopically based on morphological and pigmentation characteristics on PDA media. The morphological and pigmentation characterization of the resulting C. gloeosporioides (Figure 1) draws on literacy studies from Barnett and Hunter (1998), Semangun (2008), and Sudirga & Ketut (2016). The identification results then purified in new PDA media.
Figure 1. Colletotrichum gloeosporioides fungus. (A) Colonies on PDA media; (B) Conidia and hyphae with a size of 10.36 μm.
Isolation and identification of endophytic fungi from papaya fruit
Endophytic fungi are isolated by cutting the skin of a healthy papaya fruit with a size of 1x1x0.5 cm.
The pieces are sterilized by soaking with 2% Clorox for
a minute and rinsing using sterile aquades. After that, the pieces were dipped using 70% alcohol for 30 seconds and drained using filter paper. The dried pieces were then placed in the prepared PDA media, added
(A) (B)
80 with 0.5% chloramphenicol antibiotics, and incubated at room temperature for several days.
The grown endophytic fungal isolates were then purified in the new PDA medium and identified, which referred to Barnett and Hunter (1998). The
results of isolation, purification, and identification of endophytic fungi from papaya fruit obtained three isolates of endophytic fungi, namely Fusarium sp.
(Figure 2), Aureobasidium sp. (Figure 3), and Acremonium sp. (Figure 4).
Figure 2. Fusarium sp. (A) Colonies on PDA media; (B) Conidia.
Figure 3. Aureobasidium sp. (A) Colony on PDA media; (B) Hyphae.
Figure 4. Acremonium sp. (A) Colony on PDA media; (B) Conidia.
In-vitro test
Antagonistic fungi were tested in vitro using the dual culture method. The C. gloeosporioides and endophytic fungal isolate side by side with 3 cm on a 9 cm diameter petri dish PDA media (Figure 5). The
isolates were then incubated for ten days at room temperature. The process aims to see the inhibition and magnitude of inhibition of endophytic fungal isolates against the growth of C. gloeosporioides on PDA media.
(A) (B)
(A) (B)
(A) (B)
81 Figure 5. In-vitro antagonism test of endophytic fungi
and C. gloeosporioides fungi.
Notes: (A) Isolate of C. gloeosporioides fungi; (P) Isolate of endophytic fungi; (r1) Radius of an isolate of pathogenic fungi that stay away from antagonistic fungi; (r2) Radius of isolates of pathogenic fungi that approach the antagonistic fungi.
The number of in-vitro antagonism test treatments was three treatments of endophytic fungi (Fusarium sp., Aureobasidium sp., and Acremonium sp.) + C. gloeosporioides and a control treatment, namely pathogenic fungal isolates without endophytic fungal isolates repeated five times. Furthermore, the calculation of inhibition of endophytic fungi against C.
gloeosporioides fungi was carried out using the following equation:
I (%) =r1−r2
r1 x 100% ... (1) Notes:
I : The percentage of inhibition of antagonistic fungi to pathogens (%)
r1 : Radius isolates of pathogenic fungi that stay away from antagonistic fungi
r2 : Radius isolates of pathogenic fungi approaching antagonistic fungi
Ratnasari et al. (2014) stated that if the percentage of inhibitory power is less than 60%, then antagonistic fungi only have a minimal inhibitory effect on the growth of pathogenic fungi to attack.
Nevertheless, antagonistic fungi are said to be able to inhibit the growth of pathogenic fungi to the maximum if the percentage of inhibition is more than 60%. Only endophytic fungi with more than 60% inhibition will be tested for antagonism in-vivo.
In-vivo test
The papaya fruit used for the in-vivo antagonism test is a whole Calina variety papaya fruit aged one day after harvest. The fruit colour was 25%
orange on the fruit's skin in healthy conditions with medium size with a fruit weight of 0.8-1 kg. This in- vivo test starts by sterilizing the surface of papaya fruit by spraying 70% alcohol and drying. The papaya fruit pierced 20 punctures on the surface with a depth of 2 cm (Figure 6). Then a suspension of endophytic fungi (spores/mL) was injected into the punctured wound of 5 μL each. After it incubated for a night, 5 μL
suspension of C. gloeosporioides with 105 spore/mL density injected into each punctured wound, then stored at room temperature and observed.
Previous in-vitro test results showed that Fusarium sp. and Aurediobasidium sp. have an inhibition of more than 60%, so it is used for in-vivo tests. The in-vivo antagonism test consists of 4 treatments: C. gloeosporioides + Fusarium sp.; C.
gloeosporioides + Aureobasidium sp.; positive control (C. gloeosporioides + fungicide Antracol-Propineb 70%); negative control treatment (pathogenic fungal isolate without endophytic fungal isolate or pesticides).
The results of observing disease symptoms from in- vivo antagonism tests are then used to calculate disease intensity and inhibition of endophytic fungi. The formula calculates the intensity of the disease (%):
(Number of affected punctures: number of all punctures) x 100%
The inhibition of endophytic fungi in-vivo was calculated based on the formula:
Pv (%) = [(1-a) : b] x 100% … (2) Notes:
Pv : Percentage of inhibition of antagonistic fungi in- vivo (%)
a : The number of damage to the treatment b : The number of damage to the controls
*Endophytic fungi with an inhibitory power of more than 60% are declared capable of inhibiting C.
gloeosporioides fungi.
Figure 6. In-vivo antagonism test of endophytic fungi and C. gloeosporioides.
Data analysis
The experiment used Complete Randomized Design (RAL) with five repetitions. The data obtained were then analyzed using the ANOVA test (variety analysis) in SPSS program version 25.0. The Duncan test at a level of 5% will be used if there is a discernible difference.
RESULT AND DISCUSSIONS
In-vitro antagonism test of endophytic fungi and Colletotrichum gloeosporioides
Endophytic fungi obtained from papaya fruit Fusarium sp. and Aureobasidum sp. were able to inhibit the growth of colonies of C. gloeosporioides, while Acremonium sp. did not significantly different to inhibit from controls. The difference in the results of the inhibition of endophytic fungi against the pathogen C. gloeosporioides was based on the antagonistic
82 ability of each different fungus. Artursson et al. (2006) showed that secondary metabolites produced by antagonistic fungi can cause different fungal responses to some pathogens.
Fusarium sp. could suppress the growth of C.
gloeosporioides in-vitro by 63.5%. The antibiosis mechanism of antagonism of the fungus Fusarium sp.
can be seen from the formation of an empty zone between pathogenic and antagonistic fungi; there was also thickening in the hyphae of C. gloeosporioides (Figure 7). The antibiotic mechanism utilizes compounds produced by biocontrol agents to inhibit pathogenic hyphae that become abnormal/malformed.
Istifadah et al. (2006) found melanization and abnormalities in pathogenic hyphae due to secondary metabolites from endophytic fungi. Fusarium sp.
produces toxic secondary metabolites called mycotoxins that diffuse from hyphae to their surroundings (Burgess et al., 2006). Endophytic fungi could produce antibiotic secondary metabolites (Radji, 2005). Nitao et al. (2001) also stated that Fusarium equiseti produces antagonistic toxins to fungal pathogens and parasitic nematodes in soybean plants.
Moreover, F. equiseti can inhibit pathogenic fungi in the roots of barley plants (Maciá-Vicente et al., 2008)
.
Figure 7. Fusarium sp. antagonism test. (A) Colonies on PDA media; (B) C. gloeosporioides thickened hyphae.
Based on Table 1, Aureobasidium sp. could suppress C. gloeosporioides colonies with the highest percentage (67.86%) of inhibition compared to other treatments. The antagonism mechanism of Aureobasidium sp. is considered a competition, characterized by the fungus covering colonies of C.
gloeosporioides. In addition, Aureobasidium sp. grew
faster and filled the 9 cm petri dish (Figure 8A), whereas C. gloeosporioides hyphae undergoes lysis (Figure 8B). A. pullulans is reported to be able to compete with other microbes for space and nutrients by excreting extracellular polysaccharides, enzymes, and other molecules (Bozoudi et al., 2018).
Figure 8. Antagonism test of Aureobasidium sp. (A) Colonies on PDA media; (B) Lysis of C. gloeosporioides hyphae.
Acremonium sp. showed a low percentage of inhibition compared to other treatments at 7.52%, and the colony diameter of C. gloeosporioides almost covered the petri dish by 7.56 cm (Table 1).
Acremonium sp. was also found to slightly inhibit the growth of C. gloeosporioides which can be seen from the empty zone between the fungi (Figure 9). The
phenomenon happened because Acremonium sp.
produces secondary metabolites as an antibiotic mechanism. However, these secondary metabolites do not inhibit the growth of C. gloeosporioides. The secondary metabolites found in some Acremonium types, Cephalosporins, belong to the antibiotic and anti-inflammatory class (Zhang et al., 2009).
(A) (B)
(A) (B)
83 Grunewaldt-Stocker (2003) reports that Acremonium sp. can be an antifungal in tomato and hemp plants. Acremonium sp. could also reduce wilt symptoms due to F. oxysporum infection (Grunewaldt-
Stocker, 2003). Wicklow et al. (2005) also showed that Acremonium sp. is effectively used as an antifungal of A. flavus and F. verticillioides that produce mycotoxins.
Figure 9. Antagonism test of Acremonium sp. (A) Colonies on PDA media (B) C. gloeosporioides hyphae.
Table 1. Colletotrichum gloeosporioides colony diameter and in-vitro inhibition of endophytic fungi.
*Numbers followed by different letters in column 3 show significantly different data using the Duncan Test at a real level of 5%
In-vivo antagonism test of endophytic fungi and C.
gloeosporioides fungi
Based on the in-vivo results of the antagonism test, it can be seen that the Antracol fungicide (control negative) treatment inhibited the growth of C.
gloeosporioides by at most 100% with 0% disease intensity (Table 2; Figure 10 A). The result was in line with Sila and Sopialena (2016), which stated that Antracol fungicide has a strong disease-killing spectrum. The Antracol fungicide also slowly decomposed by the wind to more effectively suppress the development of brown spot disease on leaves and anthracnose in chilies (Sila & Sopialena, 2016).
The most effective endophytic fungal treatment in inhibiting C. gloeosporioides was the fungus Aureobasidium sp. with 97% inhibition and 3%
disease intensity (Table 2; Figure 10B). The fungus Aureobasidium sp. is reported to control pathogenic fungi from several plants. Dimakopoulou et al. (2008) state that isolation of Aureobasidium pullulans was equally effective in controlling the causes of bunch rot disease in oil palm plants. Renouf et al. (2005) also report that A. pullulans can reduce the growth of Botrytis cinerea on the surface of fresh grapes.
Fusarium sp. fungal treatment inhibits 47% with a disease intensity of 53% (Table 2). Fusarium sp.
fungus obtained from papaya fruit tissue is considered ineffective in controlling the pathogen C.
gloeosporioides that causes anthracnose disease in papaya fruit in-vivo which can be seen from the severe effect of the symptoms produced in Figure 10C.
Figure 10. Positive control treatment results on papaya fruit (C. gloeosporioides with Antracol Fungicide) (A). C.
gloeosporioides and Aureobasidium sp. treatment results on papaya fruit (B). Treatment of C. gloeosporioides with Fusarium sp. on papaya fruit. (C)
Treatment Diameter colony of
C. gloeosporioides (cm) Inhibition (%)
A Control 8.76a 0.00
B Fusarium sp. x C. gloeosporioides 5.90b 63.50
C Aureobasidum sp. x C. gloeosporioides 6.00b 67.86
D Acremonium sp. x C.gloeosporioides 7.56a 7.52
(A) (B)
A B C
84
Table 2. Growth inhibition average of Colletotrichum gloeosporioides colonies on various treatments.
*Numbers followed by different letters in column 3 show significantly different data using the Duncan Test at a real level of 5%
The effect of endophytic fungi on papaya fruit can be observed by the absence of growing colonies of C. Gloeosporioides in each hole treated. The occurrence happened because endophytic fungi could inhibit fungal growth through the antibiotic mechanisms, competition, and hyperparasitism. In line with the research of Pal and Paul (2013) that endophytic fungi can produce secondary metabolites that function as antimicrobial substances, antioxidants, cytotoxic compounds, growth hormones, and hydrolytic enzymes.
According to Burge (1988), fungi can produce various kinds of toxic compounds to fight other microorganisms. Most microorganisms produce and secrete one or more antibiotic compounds. In several studies, antibiotics produced by microorganisms are effective in suppressing pathogens that cause plant diseases (Pal & Gardener, 2006). Competition mechanisms can occur when two or more organisms have the same needs as space, nutrients, oxygen, and even light (Campbell, 1989). The mechanism of hyperparasitism occurs when antagonistic agents attack pathogens by coiling around pathogenic hyphae (Campbell, 1989).
CONCLUSIONS
Three isolates of endophytic fungi were obtained from the Calina papaya fruit tissue Fusarium sp., Aureobasidium sp., and Acremonium sp. The Fusarium sp. and Aureobasidium sp. are potential antagonistic fungal to control C. gloeosporioides pathogens, showing an average inhibition of more than 63%. Aureobasidium sp. is a potential antagonistic fungus to inhibit the colonization or growth of C.
gloeosporioides mycelium on papaya fruit, with inhibition reaching 97%.
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